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Structural Organization and Regulation of Transcription by RNA Polymerase I of Plant Nuclear Ribosomal RNA Genes

  • Conference paper
Plant Promoters and Transcription Factors

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 20))

Abstract

The RNA components of the plant cytoplasmic ribosomes consist of the 17/18S rRNA (ribosomal RNA) in the 40S ribosome subunit and the 5S, 5.8S, and 25S/26S rRNA in the 60S ribosome subunit. The corresponding genes for the 18S, 5.8S and 25S rRNA, encoded by the nuclear genome, are composed in transcription units which are located as rDNA (ribosomal DNA) repeats in the NOR (nucleolus organizing region) of the chromosome. As in higher animals, the genes for the 5S rRNA are localized separately at other regions in the genome (Hemleben and Grierson 1978). Coordinated regulation of the expression of the different components of the ribosomes can be expected since three RNA polymerases are involved to provide concomitantly the rRNA components and the mRNA for the ribosomal proteins (Sommerville 1986): RNA polymerase I (pol I) is responsible for the 18S–25S rRNA transcription, RNA polymerase III (pol III) produces the 5S rRNA, and the genes for the ribosomal proteins are transcribed by RNA polymerase II (pol II). The question how these different RNA polymerases are coordinately regulated is still a fascinating problem to solve for eukaryotic cells. Until recently, it was believed that the genes transcribed by pots I, II and III, respectively, utilize completely different sets of initiation factors; however, it has now become evident for animal cells that one common factor, the TATA-binding protein, plays a central role in transcription of all three RNA polymerases (for a review, see White and Jackson 1992).

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References

  • Agarwal ML, Aldrich J, Agarwal A, Cullis CA (1992) The flax ribosomal RNA-encoding genes are arranged in tandem at a single locus interspersed by “nonrDNA” sequences. Gene 120: 151–156

    Article  PubMed  CAS  Google Scholar 

  • Appels R, Dvorak J (1982) The wheat ribosomal DNA spacer region: its structure and variation in populations and among species. Theor Appl Genet 63: 337–348

    Article  CAS  Google Scholar 

  • Appels R, Moran LB, Gustafson JP (1986) The structrue of DNA from rye (Secale cereale) NOR R1 locus and its behaviour in wheat backgrounds. Can J Genet Cytol 28: 673–685

    CAS  Google Scholar 

  • Baerson SR, Kaufman LS (1990) Increased rRNA gene activity during a specific window of early pea leaf development. Mol Cell Biol 10: 842–845

    PubMed  CAS  Google Scholar 

  • Barker RF, Harberd NP, Jarvis MG, Flavell RB (1988) Structure and evolution of the intergenic region in a ribosomal DNA repeat unit of wheat. J Mol Biol 201: 1–17

    Article  PubMed  CAS  Google Scholar 

  • Bell SP, Pikaard CS, Reeder RH, Tijan R (1989) Molecular mechanisms governing species specific transcriptiion of ribosomal RNA. Cell 59: 489–497

    Article  PubMed  CAS  Google Scholar 

  • Bell SP, Jantzen H-M, Tjian R (1990) Assembly of alternative multiprotein complexes directs rRNA promotor selectivity. Genes Dev 4: 943–954

    Article  PubMed  CAS  Google Scholar 

  • Borisjuk N, Hemleben V (1993) Nucleotide sequence of the potato rDNA intergenic spacer. Plant Mol Biol 21: 381–384

    Article  PubMed  CAS  Google Scholar 

  • Broad JR, Li Y-Y, Feldman J, Jayaram M, Abraham J, Nasmyth KA, Hicks JB (1983) Localization and sequence analysis of yeast origins of DNA replication. Cold Spring Harbor Symp Quant Biol 47: 1165–1173

    Article  Google Scholar 

  • Capesius I, Appels R (1989) The direct measurement of ribosomal RNA gene activity in wheat-rye hybrids. Genome 32: 343–346

    Article  CAS  Google Scholar 

  • Delcasso-Tremousaygue D, Grellet F, Panabieres F, Ananiev ED, Delseny M (1988) Structural and transcriptional characterization of the external spacer of a ribosomal RNA nuclear gene from a higher plant. Eur J Biochem 172: 767–776

    Article  PubMed  CAS  Google Scholar 

  • Delseny M, Cooke R, Penon P (1983) Sequence heterogeneity in radish nuclear ribosomal RNA genes. Plant Sci Lett 30: 107–119

    Article  CAS  Google Scholar 

  • DeWinter R, Moss T (1987) A complex array of sequences enhances ribosomal transcription in Xenopus laevis. J Mol Biol 196: 813–827

    Article  CAS  Google Scholar 

  • Dover GA (1986) Molecular drive in multigene families: how biological novelties arise, spread and are assimilated. Trends Genet 2: 159–165

    Article  CAS  Google Scholar 

  • Echeverria M, Delcasso-Tremousaygue D, Delseny M (1992) A nuclear protein fraction binding to dA/dT-rich sequences upstream from the radish rDNA promoter. Plant J 2: 211–219

    PubMed  CAS  Google Scholar 

  • Ellis THN, Davies DR, Castleton JA, Bedford ID (1984) The organization and genetics of rDNA length variants in peas. Chromosoma 91: 74–81

    Article  CAS  Google Scholar 

  • Flavell RB, O’Dell M, Thompson WF (1983) Cytosine methylation of ribosomal RNA genes and nucleolus organiser activity in wheat. In: Brandham PE, Bennett MD (eds) Kew Chromosome Conference II. George Allen and Unwin, Sydney, pp 11–17

    Google Scholar 

  • Flavell RB, O’Dell M, Vincentz M, Sardana R, Barker RF (1986) The differential expression of ribosomal RNA genes. Philos Trans R Soc Lond B 314: 385–397

    Article  CAS  Google Scholar 

  • Flavell RB, O’Dell M, Thompson WF (1988) Regulation of cytosine methylation in ribosomal DNA and nucleolus organizer expression in wheat. J Mol Biol 204: 523–534

    Article  PubMed  CAS  Google Scholar 

  • Ganal M, Torres R, Hemleben V (1988) Complex structure of the ribosomal DNA spacer of Cucumis sativus (cucumber). Mol Gen Genet 212: 548–554

    Article  PubMed  CAS  Google Scholar 

  • Gerstner J, Schiebel K, von Waldburg G, Hemleben V (1988) Complex organization of the length heterogeneous 5’ external spacer of mung bean (Vigna radiata) ribosomal DNA. Genome 30: 723–733

    Article  PubMed  CAS  Google Scholar 

  • Grierson D, Loening UE (1972) Distinct transcription products of ribosomal genes in two different tissues. Nat New Biol 235: 80–82

    PubMed  CAS  Google Scholar 

  • Grierson D, Loening UE (1974) Ribosomal RNA precursors and the synthesis of chloroplast and cytoplasmic ribosomal ribonucleic acids in leaves of Phaseolus aureus. Eur J Biochem 44: 501–507

    Article  PubMed  CAS  Google Scholar 

  • Gruendler P, Unfried I, Pascher K, Schweizer D (1991) rDNA intergenic region from Arabidopsis thaliana. Structural analysis, intraspecific variation and functional implications. J Mol Biol 221: 1209–1222

    Google Scholar 

  • Grummt I, Roth E, Paule MR (1982) Ribosomal RNA transcription in vitro is species specific. Nature 296: 173–174

    Article  PubMed  CAS  Google Scholar 

  • Guilfoyle TJ, Lin CY, Chen YM, Nagao RT, Key JL (1975) Enhancement of soybean RNA polymerase I by auxin. Proc Natl Acad Sci USA 72: 69–72

    Article  PubMed  CAS  Google Scholar 

  • Hemleben V, Grierson D (1978) Evidence that in higher plants the 25S and 18S genes are not interespersed with genes for 55 rRNA. Chromosoma 65: 353–358

    Article  CAS  Google Scholar 

  • Hemleben V, Leweke B, Roth A, Stadler J (1982) Organization of highly repetitive satellite DNA from two Cucurbitaceae species (Cucumis melo and Cucumis sativus). Nucleic Acids Res 10, 631–644

    Article  PubMed  CAS  Google Scholar 

  • Hemleben V, Ganal M, Gerstner J, Schiebel K, Torres RA (1988) Organization and length heterogeneity of plant ribosomal RNA genes. In: Kahl G (ed) Architecture of eukaryotic genes. VHC, Weinheim, pp 371–383

    Google Scholar 

  • Hemleben V, Zentgraf U, King K, Borisjuk N, Schweizer G (1992) Middle repetitive and highly repetitive sequences detect polymorphisms in plants. In: Kahl G, Appelhans H, Kömpf J, Driesel AJ (eds) DNA-polymorphisms in eukaryotic genomes. BTF 10, Adv. Mol Gen 5. Huethig, Heidelberg, pp 157–170

    Google Scholar 

  • Hernandez P, Bjerknes CA, Lamm SS, Van’t Hof (1988) Proximity of an ARS consensus sequence to a replication origin of pea (Pisum sativum). Plant Mol Biol 10: 413–422

    Article  CAS  Google Scholar 

  • Ingle J, Timmis JN, Sinclair J (1975) The relationship between satellite DNA, ribosomal RNA gene redundancy, and genome size in plants. Plant Physiol 55: 496–501

    Article  PubMed  CAS  Google Scholar 

  • Jackson SD, Flavell RB (1992) Protein-binding to reiterated motifs within the wheat rRNA gene promoter and upstream repeats. Plant Mol Biol 20: 911–919

    Article  PubMed  CAS  Google Scholar 

  • Jendrisak J (1980) Purification, structures and functions of the nuclear RNA polymerases from higher plants. In: Leaver C (ed) Genome organization and expression in plants. NATO Adv Study Inst Ser: Series A, Life Sciences. Plenum Press, New York, pp 77–92

    Chapter  Google Scholar 

  • Kato A, Nakajima T, Yamashita J, Yakura K, Tanifuji S (1990) The structure of the large spacer region of the rDNA in Vicia faba and Pisum sativum. Plant Mol Biol 14: 983–993

    Article  PubMed  CAS  Google Scholar 

  • Kaufman LSJ, Watson JC, Thompson WF (1987) Light regulated changes in DNase I hypersensitive sites in the rDNA genes of Pisum sativum. Proc Natl Acad Sci USA 84: 1550–1554

    Article  PubMed  CAS  Google Scholar 

  • Kelly RJ, Siegel A (1989) The Cucurbita maxima intergenic spacer has a complex structure. Gene 80: 239–248

    Article  PubMed  CAS  Google Scholar 

  • King K, Torres RA, Zentgraf U, Hemleben V (1993) Molecular evolution of the intergenic spacer in the nuclear ribosomal RNA genes of Cucurbitaceae. J Mol Evol 36: 144–152

    Article  PubMed  CAS  Google Scholar 

  • Labhart P, Reeder RH (1987) A 12-base pair sequence is an essential element of the ribosomal gene terminator in Xenopus laevis. Mol Cell Biol 7: 1900–1905

    PubMed  CAS  Google Scholar 

  • Leweke B, Hemleben V (1982) Organization of rDNA in chromatin: plants. In: Busch H, Rothblum L (eds) The cell nucleus: rDNA. Vol XI, part B. Academic Press, New York, pp 225–253

    Google Scholar 

  • Martini G, O’Dell M, Flavell RB (1982) Partial inactivation of wheat nucleolus organisers by the nucleolus organiser chromosomes from Aegilops umbellulata. Chromosoma 84: 687–700

    Article  Google Scholar 

  • Miesfeld R, Arnheim N (1984) Species-specific rDNA transcription is due to promoter-specific binding factors. Mol Cell Biol 4: 221–227

    PubMed  CAS  Google Scholar 

  • Mitchelson K, Moss T (1987) The enhancement of ribosomal transcription by recycling of RNA polymerase I. Nucleic Acids Res 15: 9577–9596

    Article  PubMed  CAS  Google Scholar 

  • Motte PM, Loppes R, Menager M, Deltour R (1991) Three-dimensional electron microscopy of ribosomal chromatin in two higher plants: a cytochemical, immunocytochemical, and in situ hybridization approach. J Histochem Cytochem 39: 1495–1506

    Article  PubMed  CAS  Google Scholar 

  • Nakajima T, Suzuki A, Tanifuji S, Kato A (1992) Characterization of nucleotide sequences that interact with a nuclear protein fraction in rRNA gene of Vicia faba. Plant Mol Biol 20: 939–949

    Article  PubMed  CAS  Google Scholar 

  • Perry KL, Palukatis P (1990) Transcription of tomato ribosomal DNA and the organization of the intergenic spacer. Mol Gen Genet 221: 102–112

    Article  CAS  Google Scholar 

  • Perry RP (1976) Processing of RNA. Annu Rev Biochem 45: 605–629

    Article  PubMed  CAS  Google Scholar 

  • Pikaard CS, McStay B, Schultz MC, Bell SP, Reeder RH (1989) The Xenopus ribosomal gene enhancers bind an essential polymerase I transcription factor, xUBF. Genes Dev 3: 1779–1788

    Article  PubMed  CAS  Google Scholar 

  • Piller KJ, Baerson SR, Polans NO, Kaufman LS (1990) Structural analysis of the short length ribosomal DNA variant from Pisum sativum L. cv. Alaska. Nucleic Acids Res 18: 3135–3145

    Google Scholar 

  • Polans NO, Weeden HF, Thompson WF (1986) Distribution, inheritance and linkage relationship of ribosomal DNA spacer length variants in pea. Theor Appl Genet 72: 289–295

    Article  CAS  Google Scholar 

  • Rathgeber J, Capesius I (1990) Nucleotide sequence of the intergenic spacer and the 18S ribosomal RNA gene from mustard (Sinapis alba). Nucleic Acids Res 18: 1288

    Article  PubMed  CAS  Google Scholar 

  • Rogers MM, Loening UE, Fraser RSS (1970) Ribosomal RNA precursors in plants. J Mol Biol 49: 681–692

    Article  PubMed  CAS  Google Scholar 

  • Rogers SO, Bendich AJ (1987) Ribosomal RNA genes in plants: variability in copy number and in the intergenic spacer. Plant Mol Biol 9: 509–520

    Article  CAS  Google Scholar 

  • Rogers SO, Honda S, Bendich AJ (1986) Variation in the ribosomal RNA genes among individuals of Vicia faba. Plant Mol Biol 6: 339–345

    Article  CAS  Google Scholar 

  • Rungger D, Crippa M (1977) The primary ribosomal DNA transcript in eukaryotes. Proc Biopys Mol Biol 31: 247–269

    Article  CAS  Google Scholar 

  • Schiebel K, von Waldburg G, Gerstner J, Hemleben V (1989) Termination of transcription of ribosomal RNA genes of mung bean occurs within a 175 by repetitive element of the spacer region. Mol Gen Genet 218: 302–307

    Article  PubMed  CAS  Google Scholar 

  • Schmidt-Puchta W, Günther I, Sänger HL (1989) Nucleotide sequence of the inter-genic spacer ( IGS) of the tomato ribosomal DNA. Plant Mol Biol 13: 251–253

    Google Scholar 

  • Schmitz ML, Maier UG, Brown JWS, Feix G (1989) Specific binding of nuclear proteins to the promoter region of a maize nuclear rRNA gene unit. J Biol Chem 264: 1467–1472

    PubMed  CAS  Google Scholar 

  • Scott NS, Kavanagh TA, Timmis JN (1984) Methylation of rRNA genes in some higher plants. Plant Sci Lett 35: 213–217

    Article  CAS  Google Scholar 

  • Shagai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81: 8014–8018

    Google Scholar 

  • Sollner-Webb B, Mougey EB (1991) News from the nucleolus: rRNA gene expression. Trends Biochem Sci 16: 58–62

    Article  PubMed  Google Scholar 

  • Sollner-Webb B, Tower J (1986) Transcription of cloned eukaryotic ribosomal RNA genes. Annu Rev Biochem 55: 801–830

    Article  PubMed  CAS  Google Scholar 

  • Sommerville J (1986) Nucleolar structure and ribosome biosynthesis. Trends Biochem Sci 11: 438–442

    Article  CAS  Google Scholar 

  • Spiker S, Murray MG, Thompson WF (1983) DNase I sensitivity of transcriptionally active genes in intact nuclei and isolated chromatin of plants. Proc Natl Acad Sci USA 80: 815–819

    Article  PubMed  CAS  Google Scholar 

  • Tautz D, Tautz C, Webb D, Dover GA (1987) Evolutionary divergence of promoters and spacers in the rDNA family of four Drosophila species. J Mol Biol 195: 525–542

    Article  PubMed  CAS  Google Scholar 

  • Thompson WF, Flavell RB (1988) DNase I sensitivity of ribosomal RNA genes in chromatin and nucleolar dominance in wheat. J Mol Biol 204: 535–548

    Article  PubMed  CAS  Google Scholar 

  • Thompson WF, Flavell RB, Watson JC, Kaufman LS (1988) Chromatin structure and expression of plant ribosomal RNA genes. In: Kahl G (ed) Architecture of eukaryotic genes. VCH, Weinheim, pp 385–396

    Google Scholar 

  • Tobin EM, Silverthorne (1985) Light regulation of gene expression in higher plants. Annu Rev Plant Physiol 36: 569–593

    Article  CAS  Google Scholar 

  • Toloczyki C, Feix G (1986) Occurrence of 9 homologous repeat units in the external spacer region of a nuclear maize rRNA gene unit. Nucleic Acids Res 14: 4969–4986

    Article  PubMed  CAS  Google Scholar 

  • Torres RA, Hemleben V (1991) Use of ribosomal DNA spacer probes to distinguish cultivars of Cucurbita pepo L. and other Cucurbitaceae. Euphytica 53: 11–17

    Article  Google Scholar 

  • Torres RA, Zentgraf U, Hemleben V (1989) Species and genus specificity of the intergenic spacer ( IGS) in the ribosomal RNA genes of Cucurbitaceae. Z Naturforsch 44c: 1029–1034

    Google Scholar 

  • Torres RA, Ganal M, Hemleben V (1990) GC balance in the internal transcribed spacers ITS 1 and ITS 2 of nuclear ribosomal RNA genes. J Mol Evol 30: 170–181

    Article  PubMed  CAS  Google Scholar 

  • Ueki M, Uchizawa E, Yakura K (1992) The nucleotide sequence of the rDNA intergenic spacer region in a wild species of the genus Vicia, V. angustifolia. Plant Mol Biol 18: 175–178

    Article  PubMed  CAS  Google Scholar 

  • Unfried K, Schiebel K, Hemleben V (1991) Subrepeats of rDNA intergenic spacer present as prominent independent satellite DNA in Vigna radiata but not in Vigna angularis. Gene 99: 63–68

    Article  PubMed  CAS  Google Scholar 

  • Van’t Hof J, Lamm SS (1992) Site of initiation of replication of the ribosomal genes of pea (Pisum sativum) detected by two-dimensional gel electrophoresis. Plant Mol Biol 20: 377–382

    Article  Google Scholar 

  • Vincentz M, Flavell RB (1989) Mapping of ribosomal RNA transcripts in wheat. Plant Cell 1: 579–589

    PubMed  CAS  Google Scholar 

  • Von Kalm L, Vize PD, Smyth DR (1986) An under methylated region in the spacer of ribosomal RNA genes of Lilium henryi. Plant Mol Biol 6: 33–39

    Article  Google Scholar 

  • Weising K, Kahl G (1991) Towards an understanding of plant gene regulation: the action of nuclear factors. Z Naturforsch 46c: 1–11

    CAS  Google Scholar 

  • White RJ, Jackson SP (1992) The TATA-binding protein: a central role in transcription by RNA polymerase I, II and III. Trends Genet 8: 284–288

    Google Scholar 

  • Yakura K, Nishikawa K (1992) The nucleotide sequence of the rDNA spacer region between the 25S and 18S rRNA genes in a species of the genus Vicia, V. hirsuta. Plant Mol Biol 19: 537–539

    Article  PubMed  CAS  Google Scholar 

  • Yakura K, Kato A, Tanifuji S (1983) Structural organization of ribosomal DNA in four Trillium species and Paris verticillata. Plant Cell Physiol 24: 1231–1240

    CAS  Google Scholar 

  • Yamashita J, Nakajima T, Tanifuij S, Kato A (1993) Accurate transcription initiation of Vicia faba rDNA in a whole cell extract from embryonic axes. Plant J 3: 187–190

    Article  CAS  Google Scholar 

  • Yang-Yen H-F, Rothblum L (1988) Purification and characterization of a highmobility-group-like DNA-binding protein that stimulates rRNA sythesis in vitro. Mol Cell Biol 8: 3406–3414

    PubMed  CAS  Google Scholar 

  • Zentgraf U, Hemleben V (1992) Complex formation of nuclear proteins with the RNA polymerase I promoter and repeated elements in the external transcribed spacer of Cucumis sativus ribosomal DNA. Nucleic Acids Res 20: 3685–3691

    Article  PubMed  CAS  Google Scholar 

  • Zentgraf U, Hemleben V (1993) Nuclear Proteins interact with RNA polymerase I promoter and repeated elements of the 5’ external transcribed spacer of the rDNA of cucumber in a single-stranded stage. Plant Mol Biol 22: 1153–1156

    Article  PubMed  CAS  Google Scholar 

  • Zentgraf U, Ganal M, Hemleben V (1990) Length heterogeneity of the rRNA precursor in cucumber (Cucumis sativus). Plant Mol Biol 15: 465–474

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Genetics, Biological Institute, University of Tübingen, Auf der Morgenstelle 28, D-72076, Tübingen, Germany

    Vera Hemleben & Ulrike Zentgraf

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  1. Vera Hemleben
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  2. Ulrike Zentgraf
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  1. Dept. of Molecular Cell Biology, University of Frankfurt Biocenter, Marie-Curie-Straße 9, D-60439, Frankfurt, Germany

    Lutz Nover

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Hemleben, V., Zentgraf, U. (1994). Structural Organization and Regulation of Transcription by RNA Polymerase I of Plant Nuclear Ribosomal RNA Genes. In: Nover, L. (eds) Plant Promoters and Transcription Factors. Results and Problems in Cell Differentiation, vol 20. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-48037-2_1

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  • DOI: https://doi.org/10.1007/978-3-540-48037-2_1

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